Investigation of Francisella tularensis Seroprevalence and Determination of Risk Factors for Tularemia among Hunters in Northern Cyprus
,
Abstract
Background: Tularemia is a zoonotic disease (reservoir is usually rodents) caused by Francisella tularensis, especially seen in the northern hemisphere. Hunters are in the risk group for this disease. In this study, it was aimed to determine the seroprevalence of tularemia among hunters and determine the risk factors of tularemia in our country.
Methods: The Turkish Republic of Northern Cyprus (TRNC) is divided into four regions (Nicosia, Kyrenia, Famagusta/Trikomo, and Morphou/Lefka) and 100 volunteer hunters randomly selected from these regions were included in our study. Tube agglutination test (TAT) and F. tularensis IgG and IgM (ELISA method) were applied in all sera. All hunters were filled with a pre-prepared questionnaire to determine risk factors for tularemia.
Results: TAT positivity was found in 11%. While F. tularensis ELISA IgG positivity was 17%, IgM positivity was not found in any hunters. Hunters with positive F. tularensis ELISA IgG test (17%) were accepted as seropositive in terms of tularemia. There was no statistically significant difference between the mean age of IgG-positive and negative hunters (p= 0.915). Of the 86 hunters who kept at least one hunting dog in their garden, 15 (17.4%) were IgG-positive. There was no significant relationship between feeding hunting dogs and tularemia (p= 0.561).
Conclusion: Our study showed that the seroprevalence of tularemia was high (17%) among hunters, who are considered a risk group, in our country. We think that more epidemiological research should be done on tularemia infection and it should not be overlooked in the clinic.
1. Obaidat MM, Malania L, Bani Salman AE, Arner RJ, Roess AA (2020) Seroepide-miolo¬gy, Spatial distribution, and risk factors of Francisella tularensis in Jor-dan. Am J Trop Med Hyg. 103(2): 659‒664.
2. Büyük F, Çelebi Ö, Çelik E, Çelebi B, Kiliç S, Gülmez Sağlam A, Akça D, Doğanay M, Otlu S, Şahin M (2016) The preva-lence of tularemia in occupa¬tional groups that have contact with an¬imals. Turk J Med Sci. 46(2): 451‒456.
3. Boz A, Aktuna G, Özgülcü Ş, Sezgin B, Temel F, Çelebi B (2016) Tularemia cases in Dinar District, Afyonkarahisar Prov¬ince, Janu¬ary 2015. Turk Hij Den Biyol Derg. 73(3): 233‒244.
4. Esmaeili S, Ghasemi A, Naserifar R, Jalilian A, Molaeipoor L, Maurin M, Mosta¬favi E (2019) Epidemiological survey of tu¬la-remia in Ilam Province, west of Iran. BMC Infect Dis. 19(1): 502.
5. Bayındır T, Can Ş, Bayındır Y, Kızılay A (2014) Tularemia. Bozok Med J. 1(1): 54‒59.
6. Hestvik G, Warns-Petit E, Smith LA, Fox NJ, Uhlhorn H, Artois M, Hannant D, Hutch¬ings MR, Mattsson R, Yon L, Gavi¬er-Widen D (2015) The status of tulare¬mia in Europe in a one-health con-text: a review. Epidemiol In¬fect. 143: 2137‒2160.
7. Aktepe E, Sönmezer MÇ, Yarımoğlu S, Erdinç FŞ, Ertem G, Tülek N (2017) De¬layed diagnosis of ulceroglandular Tula¬remia: A case report. Klimik Derg. 30(2): 83‒86.
8. Uncu M, Süer K, Kocaoğlu M, Şafak MA, Çağlar K (2017) Case report of systemic Tu¬laremia in Cyprus. Cyprus J Med Sci. 2(3): 81‒84.
9. Karataş Yeni D, Büyük F, Ashraf A, Ud Din Shah MS (2021) Tularemia: a re-emerging tick-borne infectious diseases. Folia Microbiol. 66(1): 1‒14.
10. Gürcan Ş (2014) Epidemiology of Tula-remia. Balkan Med J. 31: 3‒10.
11. Esmaeili S, Gooya MM, Shirzadi MR, Esfan¬diari B, Amiri FB, Behzadi MY, Banaf¬shi O, Mostafavi E (2014) Seroep-idemiologi¬cal survey of tularemia among different groups in western Iran. Int J In¬fect Dis. 18: 27‒31.
12. Önen S, Paksoy, Dallar Bilge Y (2012) Tularemia cases in childhood. J Pediatr Inf. 6: 94‒100.
13. Arslanyılmaz M, Aslan D, Akın L, Aktaş D (2014) Updated assessment on tula-remia. Turk Hij Den Biyol Derg. 71(2): 99‒106.
14. European Centre for Disease Prevention and Control (ECDC) (2016) Tularemia-Annual Epidemiological Report 2016 [2014 data]. Available at: https://www.ecdc.europa.eu/sites/default/files/documents/Tularaemia%20AER_0.pdf.
15. Turkish Republic of Northern Cyprus Min¬istry of Health. Statistical Infor-mations, Notifiable Diseases. Available at: http://www.saglik.gov.ct.tr/İSTATİSTİKİ-BİLGİLER/Bildirimi-Zorunlu-Hastalıklar.
16. Karataş Yeni D, Ruh E, Bostancı A, Çelebi B, Taylan Özkan HA (2022) In-vestiga¬tion of Seropositivity of Tularemia, Bru¬cellosis and Leptospirosis in Hu¬mans in Northern Cyprus. Fresenius Envi¬ronmental Bulletin. https://hdl.handle.net/20.500.11851/10067.
17. Turkish Republic of Northern Cyprus Hunt¬ing Federation. About us, History. Avail¬able at: http://www.avfed.com/hakkimizda.htm
18. Şenol C (2020) The Turkish Republic of North¬ern Cyprus Hydrographic Struc-ture, Water Problem and Solution Sug-gestions. JCS. 21(45): 77‒98.
19. TRNC Public Information Office. Geo-graphic Information. Available at: https://pio.mfa.gov.ct.tr/en/geographic-information/
20. Helvacı S, Gedikoğlu S, Akalın H, Oral HB (2000) Tularemia in Bursa, Turkey: 205 cases in ten years. Eur J Epidemiol. 16: 271‒276.
21. World Health Organization (2007) WHO Guidelines on Tularaemia. Available at: https://iris.who.int/bitstream/handle/10665/43793/9789241547376_eng.pdf?sequence=1&isAllowed=y.
22. Bayram Y, Özkaçmaz A, Parlak M, Başbuğan Y, Kılıç S, Güdücüoğlu H (2015) Seroprevalence of tularemia in risk groups of humans and animals in Van, East of Turkey. Mikrobiyol Bul. 49(4): 532‒541.
23. Uyar-Güleç G (2019) Delayed diagnosis of tularemia in a nonendemic area: A re-port of three cases. Klimik Derg. 32(2): 206‒209.
24. Köse H, Temoçin F, Sarı T (2020) Tula-remia outbreak and after; effect of sea-son¬al changes. Mikrobiyol Bul. 54(2): 203‒ 210.
25. Jenzora A, Jansen A, Ranisch H, Lierz M, Wichmann O, Grunow R (2008) Sero-preva¬lence study of Francisela tularen-sis among hunters in Germany. FEMS Im¬munol Med Microbiol. 53: 183‒189.
26. Rossow H, Ollgren J, Hytönen J, Rissanen H, Huitu O, Henttonen H, Kuusi M, Vapalahti O (2015) Incidence and sero-prevalence of tu¬laraemia in Finland, 1995 to 2013: regional epidemics with cyclic pattern. Euro Surveill. 20(33): 21209.
27. De Keukeleire M, Vanwambeke SO, Co-chez C, Heyman P, Fretin D, Deneys V, Luyasu V, Kabamba B, Robert A (2017) Se¬roprevalence of Borrelia burgdorferi, Ana¬plasma phagocytophilum, and Fran-cisella tu¬laren¬sis infections in Belgium: Results of three population-based sam-ples. Vector Borne Zoonotic Dis. 17(2): 108‒115.
28. Tobudic S, Nedomansky K, Poeppl W, Mül¬ler M, Faas A, Mooseder G, Aller-berger F, Stanek G, Burgmann H (2014) Sero¬preva¬lence for Coxiella burnetii, Fran¬cisella tu¬laren¬sis, Brucella abortus, and Brucella melitensis in Austrian adults: A cross-sectional survey among military personnel and civilians. Ticks Tick Borne Dis. 5(3): 315‒317.
29. Yazgı H, Uyanık MH, Ertek M, Kılıç S, Kireçci E, Ozden K, Ayyıldız A (2011) Tula¬remia seroprevalence in the risky popula¬tion living in both rural and urban areas of Erzu¬rum. Mikrobiyol Bul. 45 (1): 67‒74.
30. Yeşilyurt M, Kılıç S, Çelebi B, Gül S (2012) Tularemia: Are hunters really a risk group?. Microbiyol Bul. 46(1): 153‒155.
31. Tokarska-Rodak M, Weiner M, Szyman-ska-Czerwinska M, Panczuk A, Niemczuk K, Sroka J, Rozycki M, Iwaniak W (2018) Sero¬prevalence of se-lected zoonotic agents among hunters from Eastern Poland. Pol J Microbiol. 67(2): 233‒236.
32. Clark DV, Ismailov A, Seyidova E, Haji-yeva A, Bakhishova S, Hajiyev H, Nu-riyev T, Piraliyev S, Bagirov S, Aslano-va A, Debes AK, Qasimov M, Hepburn MJ (2012) Sero¬prevalence of tularemia in rural Azerbaijan. Vector Borne Zoon-otic Dis. 12(7): 558‒563.
33. Kılıç S, Çelebi B, Bayram Y, Çitil B (2013) Investigation of cross-reactions with Fran¬cisella tularensis antibodies to Brucella. Turk Hij Den Biyol Derg. 70(2): 65‒70.
34. Francis E, Evans AC (1926) Agglutina-tion, cross-agglutination, and agglutinin ab¬sorption in Tularaemia. Public Health Rep. 41(26): 1273‒1295.
35. Maurin M (2020) Francisella tularensis, tularemia and serological diagnosis. Front Cell Infect Microbiol. 10: 512090.
36. Behan KA, Klein GC (1982) Reduction of Brucella species and Francisella tu-laren¬sis cross-reacting agglutinins by di-thio¬threitol. J Clin Microbiol. 16(4): 756‒757.
2. Büyük F, Çelebi Ö, Çelik E, Çelebi B, Kiliç S, Gülmez Sağlam A, Akça D, Doğanay M, Otlu S, Şahin M (2016) The preva-lence of tularemia in occupa¬tional groups that have contact with an¬imals. Turk J Med Sci. 46(2): 451‒456.
3. Boz A, Aktuna G, Özgülcü Ş, Sezgin B, Temel F, Çelebi B (2016) Tularemia cases in Dinar District, Afyonkarahisar Prov¬ince, Janu¬ary 2015. Turk Hij Den Biyol Derg. 73(3): 233‒244.
4. Esmaeili S, Ghasemi A, Naserifar R, Jalilian A, Molaeipoor L, Maurin M, Mosta¬favi E (2019) Epidemiological survey of tu¬la-remia in Ilam Province, west of Iran. BMC Infect Dis. 19(1): 502.
5. Bayındır T, Can Ş, Bayındır Y, Kızılay A (2014) Tularemia. Bozok Med J. 1(1): 54‒59.
6. Hestvik G, Warns-Petit E, Smith LA, Fox NJ, Uhlhorn H, Artois M, Hannant D, Hutch¬ings MR, Mattsson R, Yon L, Gavi¬er-Widen D (2015) The status of tulare¬mia in Europe in a one-health con-text: a review. Epidemiol In¬fect. 143: 2137‒2160.
7. Aktepe E, Sönmezer MÇ, Yarımoğlu S, Erdinç FŞ, Ertem G, Tülek N (2017) De¬layed diagnosis of ulceroglandular Tula¬remia: A case report. Klimik Derg. 30(2): 83‒86.
8. Uncu M, Süer K, Kocaoğlu M, Şafak MA, Çağlar K (2017) Case report of systemic Tu¬laremia in Cyprus. Cyprus J Med Sci. 2(3): 81‒84.
9. Karataş Yeni D, Büyük F, Ashraf A, Ud Din Shah MS (2021) Tularemia: a re-emerging tick-borne infectious diseases. Folia Microbiol. 66(1): 1‒14.
10. Gürcan Ş (2014) Epidemiology of Tula-remia. Balkan Med J. 31: 3‒10.
11. Esmaeili S, Gooya MM, Shirzadi MR, Esfan¬diari B, Amiri FB, Behzadi MY, Banaf¬shi O, Mostafavi E (2014) Seroep-idemiologi¬cal survey of tularemia among different groups in western Iran. Int J In¬fect Dis. 18: 27‒31.
12. Önen S, Paksoy, Dallar Bilge Y (2012) Tularemia cases in childhood. J Pediatr Inf. 6: 94‒100.
13. Arslanyılmaz M, Aslan D, Akın L, Aktaş D (2014) Updated assessment on tula-remia. Turk Hij Den Biyol Derg. 71(2): 99‒106.
14. European Centre for Disease Prevention and Control (ECDC) (2016) Tularemia-Annual Epidemiological Report 2016 [2014 data]. Available at: https://www.ecdc.europa.eu/sites/default/files/documents/Tularaemia%20AER_0.pdf.
15. Turkish Republic of Northern Cyprus Min¬istry of Health. Statistical Infor-mations, Notifiable Diseases. Available at: http://www.saglik.gov.ct.tr/İSTATİSTİKİ-BİLGİLER/Bildirimi-Zorunlu-Hastalıklar.
16. Karataş Yeni D, Ruh E, Bostancı A, Çelebi B, Taylan Özkan HA (2022) In-vestiga¬tion of Seropositivity of Tularemia, Bru¬cellosis and Leptospirosis in Hu¬mans in Northern Cyprus. Fresenius Envi¬ronmental Bulletin. https://hdl.handle.net/20.500.11851/10067.
17. Turkish Republic of Northern Cyprus Hunt¬ing Federation. About us, History. Avail¬able at: http://www.avfed.com/hakkimizda.htm
18. Şenol C (2020) The Turkish Republic of North¬ern Cyprus Hydrographic Struc-ture, Water Problem and Solution Sug-gestions. JCS. 21(45): 77‒98.
19. TRNC Public Information Office. Geo-graphic Information. Available at: https://pio.mfa.gov.ct.tr/en/geographic-information/
20. Helvacı S, Gedikoğlu S, Akalın H, Oral HB (2000) Tularemia in Bursa, Turkey: 205 cases in ten years. Eur J Epidemiol. 16: 271‒276.
21. World Health Organization (2007) WHO Guidelines on Tularaemia. Available at: https://iris.who.int/bitstream/handle/10665/43793/9789241547376_eng.pdf?sequence=1&isAllowed=y.
22. Bayram Y, Özkaçmaz A, Parlak M, Başbuğan Y, Kılıç S, Güdücüoğlu H (2015) Seroprevalence of tularemia in risk groups of humans and animals in Van, East of Turkey. Mikrobiyol Bul. 49(4): 532‒541.
23. Uyar-Güleç G (2019) Delayed diagnosis of tularemia in a nonendemic area: A re-port of three cases. Klimik Derg. 32(2): 206‒209.
24. Köse H, Temoçin F, Sarı T (2020) Tula-remia outbreak and after; effect of sea-son¬al changes. Mikrobiyol Bul. 54(2): 203‒ 210.
25. Jenzora A, Jansen A, Ranisch H, Lierz M, Wichmann O, Grunow R (2008) Sero-preva¬lence study of Francisela tularen-sis among hunters in Germany. FEMS Im¬munol Med Microbiol. 53: 183‒189.
26. Rossow H, Ollgren J, Hytönen J, Rissanen H, Huitu O, Henttonen H, Kuusi M, Vapalahti O (2015) Incidence and sero-prevalence of tu¬laraemia in Finland, 1995 to 2013: regional epidemics with cyclic pattern. Euro Surveill. 20(33): 21209.
27. De Keukeleire M, Vanwambeke SO, Co-chez C, Heyman P, Fretin D, Deneys V, Luyasu V, Kabamba B, Robert A (2017) Se¬roprevalence of Borrelia burgdorferi, Ana¬plasma phagocytophilum, and Fran-cisella tu¬laren¬sis infections in Belgium: Results of three population-based sam-ples. Vector Borne Zoonotic Dis. 17(2): 108‒115.
28. Tobudic S, Nedomansky K, Poeppl W, Mül¬ler M, Faas A, Mooseder G, Aller-berger F, Stanek G, Burgmann H (2014) Sero¬preva¬lence for Coxiella burnetii, Fran¬cisella tu¬laren¬sis, Brucella abortus, and Brucella melitensis in Austrian adults: A cross-sectional survey among military personnel and civilians. Ticks Tick Borne Dis. 5(3): 315‒317.
29. Yazgı H, Uyanık MH, Ertek M, Kılıç S, Kireçci E, Ozden K, Ayyıldız A (2011) Tula¬remia seroprevalence in the risky popula¬tion living in both rural and urban areas of Erzu¬rum. Mikrobiyol Bul. 45 (1): 67‒74.
30. Yeşilyurt M, Kılıç S, Çelebi B, Gül S (2012) Tularemia: Are hunters really a risk group?. Microbiyol Bul. 46(1): 153‒155.
31. Tokarska-Rodak M, Weiner M, Szyman-ska-Czerwinska M, Panczuk A, Niemczuk K, Sroka J, Rozycki M, Iwaniak W (2018) Sero¬prevalence of se-lected zoonotic agents among hunters from Eastern Poland. Pol J Microbiol. 67(2): 233‒236.
32. Clark DV, Ismailov A, Seyidova E, Haji-yeva A, Bakhishova S, Hajiyev H, Nu-riyev T, Piraliyev S, Bagirov S, Aslano-va A, Debes AK, Qasimov M, Hepburn MJ (2012) Sero¬prevalence of tularemia in rural Azerbaijan. Vector Borne Zoon-otic Dis. 12(7): 558‒563.
33. Kılıç S, Çelebi B, Bayram Y, Çitil B (2013) Investigation of cross-reactions with Fran¬cisella tularensis antibodies to Brucella. Turk Hij Den Biyol Derg. 70(2): 65‒70.
34. Francis E, Evans AC (1926) Agglutina-tion, cross-agglutination, and agglutinin ab¬sorption in Tularaemia. Public Health Rep. 41(26): 1273‒1295.
35. Maurin M (2020) Francisella tularensis, tularemia and serological diagnosis. Front Cell Infect Microbiol. 10: 512090.
36. Behan KA, Klein GC (1982) Reduction of Brucella species and Francisella tu-laren¬sis cross-reacting agglutinins by di-thio¬threitol. J Clin Microbiol. 16(4): 756‒757.
| Files | ||
| Issue | Vol 18 No 1 (2024) | |
| Section | Original Article | |
| DOI | https://doi.org/10.18502/jad.v18i1.15671 | |
| Keywords | ||
| Tularemia Francisella tularensis Northern Cyprus Seroprevalenve Hunters | ||
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How to Cite
1.
Güler E, Güvenir M, Korbay B, Kiraz A, Süer K. Investigation of Francisella tularensis Seroprevalence and Determination of Risk Factors for Tularemia among Hunters in Northern Cyprus. J Arthropod Borne Dis. 2024;18(1):47–56.
